1887

Abstract

Slr1295 (and Slr0513) in the cyanobacterium sp. PCC 6803 has amino acid similarity to the bacterial FbpA protein family and also to IdiA of PCC 6301/PCC 7942. To determine whether Slr1295 is the periplasm-located component of an iron transporter, or has a function in protecting photosystem (PS) II, subcellular localization and Δmutant characterization studies were performed. Localization of Slr1295 provided evidence that it has an intracellular function, since virtually no Slr1295 was detected in the soluble protein fraction of the periplasm or in the cytoplasmic membrane. Characterization of a Δ PCC 6803 mutant indicated that PS II is more susceptible to inactivation in the mutant than in the wild-type (WT). Under mild iron limitation, modification of PS I to the PS I–IsiA complex is more advanced in the Δmutant, indicating that iron deficiency leads more rapidly to changes in the photosynthetic apparatus in the mutant than in the WT. Biochemical fractionation procedures provide evidence that Slr1295 co-purifies with PS II. These results suggest a function of Slr1295 that is comparable to the function of IdiA in PCC 6301/PCC 7942 being a protein that protects PS II under iron limitation in an as yet unknown way.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-10-3293
2002-10-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/10/1483293a.html?itemId=/content/journal/micro/10.1099/00221287-148-10-3293&mimeType=html&fmt=ahah

References

  1. Adhikari, P., Berish, S. A., Nowalk, A. J., Veraldi, K. L., Morse, S. A. & Mietzner, T. A. ( 1996; ). The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron. J Bacteriol 178, 2145-2149.
    [Google Scholar]
  2. Angerer, A., Gaisser, S. & Braun, V. ( 1990; ). Nucleotide sequences of the sufA, sfuB, and sfuC genes of Serratia marcescens suggest a periplasmic-binding-protein-dependent iron transport mechanism. J Bacteriol 172, 572-578.
    [Google Scholar]
  3. Aro, E. M., Virgin, I. & Andersson, B. ( 1993; ). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143, 113-134.[CrossRef]
    [Google Scholar]
  4. Behrenfeld, M. J. & Kolber, Z. S. ( 1999; ). Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283, 840-843.[CrossRef]
    [Google Scholar]
  5. Berish, S. A., Mietzner, T. A., Mayer, L. W., Genco, C. A., Holloway, B. P. & Morse, S. A. ( 1990a; ). Molecular cloning and characterization of the structural gene for the major iron-regulated protein expressed by Neisseria gonorrhoeae. J Exp Med 171, 1535-1546.[CrossRef]
    [Google Scholar]
  6. Berish, S. A., Kapczynski, D. R. & Morse, S. A. ( 1990b; ). Nucleotide sequence of the Fbp gene from Neisseria meningitidis. Nucleic Acids Res 18, 4596.[CrossRef]
    [Google Scholar]
  7. Berks, B. C. ( 1996; ). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22, 393-404.[CrossRef]
    [Google Scholar]
  8. Berks, B. C., Sargent, F. & Palmer, T. ( 2000; ). The Tat protein export pathway. Mol Microbiol 35, 260-274.[CrossRef]
    [Google Scholar]
  9. Bibby, T. S., Nield, J. & Barber, J. ( 2001a; ). Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412, 743-745.[CrossRef]
    [Google Scholar]
  10. Bibby, T. S., Nield, J. & Barber, J. ( 2001b; ). Three-dimensional model and characterization of the iron-stress-induced CP43′-photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803. J Biol Chem 276, 43246-43252.[CrossRef]
    [Google Scholar]
  11. Block, M. A. & Grossman, A. R. ( 1988; ). Identification and purification of a derepressible alkaline phosphatase from Anacystis nidulans R2. Plant Physiol 86, 1179-1184.[CrossRef]
    [Google Scholar]
  12. Boekema, E. J., Hifney, A., Yakushevska, A. E., Piotrowski, M., Keegstra, W., Berry, S., Michel, K.-P., Pistorius, E. K. & Kruip, J. ( 2001; ). A giant chlorophyll-protein complex induced by iron deficiency. Nature 412, 745-748.[CrossRef]
    [Google Scholar]
  13. Bradford, M. M. ( 1976; ). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72, 248-254.[CrossRef]
    [Google Scholar]
  14. Brink, S., Bogsch, E. G., Edwards, W. R., Hynds, P. J. & Robinson, C. ( 1998; ). Targeting of thylakoid proteins by the ΔpH-driven twin-arginine translocation pathway requires a specific signal in the hydrophobic domain in conjunction with the twin-arginine motif. FEBS Lett 434, 425-430.[CrossRef]
    [Google Scholar]
  15. Burnap, R., Koike, H., Sotiropoulou, G., Sherman, L. A. & Inoue, Y. ( 1989; ). Oxygen evolving membranes and particles from the transformable cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 22, 123-130.[CrossRef]
    [Google Scholar]
  16. Burnap, R. L., Troyan, T. & Sherman, L. A. ( 1993; ). The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC 7942 (CP43′) is encoded by the isiA gene. Plant Physiol 103, 893-902.[CrossRef]
    [Google Scholar]
  17. Chang, A. C. Y. & Cohen, S. N. ( 1978; ). Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134, 1141-1156.
    [Google Scholar]
  18. Downs, C. A., Coleman, J. S. & Heckathorn, S. A. ( 1999a; ). The chloroplast 22-Ku heat-shock protein: a lumenal protein that associates with the oxygen evolving complex and protects photosystem II during heat stress. J Plant Physiol 155, 477-487.[CrossRef]
    [Google Scholar]
  19. Downs, C. A., Ryan, S. L. & Heckathorn, S. A. ( 1999b; ). The chloroplast small heat-shock protein: evidence for a general role in protecting photosystem II against oxidative stress and photoinhibition. J Plant Physiol 155, 488-496.[CrossRef]
    [Google Scholar]
  20. Engels, A., Kahmann, U., Ruppel, H. G. & Pistorius, E. K. ( 1997; ). Isolation, partial characterization and localisation of a dihydrolipoamide dehydrogenase from the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1340, 33-44.[CrossRef]
    [Google Scholar]
  21. Exss-Sonne, P., Tölle, J., Bader, K. P., Pistorius, E. K. & Michel, K.-P. ( 2000; ). The IdiA protein of Synechococcus sp. PCC 7942 functions in protecting the acceptor side of photosystem II under oxidative stress. Photosynth Res 63, 145-157.[CrossRef]
    [Google Scholar]
  22. Falk, S., Samson, G., Bruce, D., Huner, N. P. A. & Laudenbach, D. E. ( 1995; ). Functional analysis of the iron-stress induced CP43′ polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 45, 51-60.[CrossRef]
    [Google Scholar]
  23. Ferreira, F. & Straus, N. A. ( 1994; ). Iron deprivation in cyanobacteria. J Appl Phycol 6, 199-210.[CrossRef]
    [Google Scholar]
  24. Flores, E., Herrero, A. & Guerrero, M. G. ( 1982; ). Production of ammonium dependent on basic l-amino acids by Anacystis nidulans. Arch Microbiol 131, 91-94.[CrossRef]
    [Google Scholar]
  25. Forng, R.-Y., Ekechukwu, C. R., Subbarao, S., Morse, S. A. & Genco, C. A. ( 1997; ). Promoter mapping and transcriptional regulation of the iron-regulated Neisseria gonorrhoeae fbpA gene. J Bacteriol 179, 3047-3052.
    [Google Scholar]
  26. Fulda, S., Huang, F., Nilsson, F., Hagemann, M. & Norling, B. ( 2000; ). Proteomics of Synechocystis sp. strain PCC 6803. Eur J Biochem 267, 5900-5907.[CrossRef]
    [Google Scholar]
  27. Geider, R. J. & La Roche, J. ( 1994; ). The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth Res 39, 275-301.[CrossRef]
    [Google Scholar]
  28. Grimme, L. H. & Boardman, N. K. ( 1972; ). Photochemical activities of a particle fraction P1 obtained from the green alga Chlorella fusca. Biochem Biophys Res Commun 49, 1617-1620.[CrossRef]
    [Google Scholar]
  29. Halbig, D., Hou, B., Freudl, R., Sprenger, G. A. & Klösgen, R. B. ( 1999; ). Bacterial proteins carrying twin-R signal peptides are specifically targeted by the ΔpH-dependent transport machinery of the thylakoid membrane system. FEBS Lett 447, 95-98.[CrossRef]
    [Google Scholar]
  30. Kaneko, T., Sato, S., Kotani, H. & 21 other authors ( 1996; ). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3, 109–136.[CrossRef]
    [Google Scholar]
  31. Katoh, H., Grossman, A. R., Hagino, N. & Ogawa, T. ( 2000; ). A gene of Synechocystis sp. strain PCC 6803 encoding a novel iron transporter. J Bacteriol 182, 6523-6524.[CrossRef]
    [Google Scholar]
  32. Katoh, H., Hagino, N., Grossman, A. R. & Ogawa, T. ( 2001a; ). Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183, 2779-2784.[CrossRef]
    [Google Scholar]
  33. Katoh, H., Hagino, N. & Ogawa, T. ( 2001b; ). Iron-binding activity of FutA1 subunit of an ABC-type iron transporter in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Cell Physiol 42, 823-827.[CrossRef]
    [Google Scholar]
  34. Ke, B. (2001). The primary electron donor of photosystem II, P680, and photoinhibition. In Photosynthesis, Photobiochemistry and Photobiophysics, Advances in Photosynthesis, Vol. 10, pp. 271–288, Dordrecht: Kluwer.
  35. Kirby, S. D., Lainson, F. A., Donachie, W., Okabe, A., Tokuda, M., Hatase, O. & Schryvers, A. B. ( 1998; ). The Pasteurella haemolytica 35 kDa iron-regulated protein is an FbpA homologue. Microbiology 144, 3425-3436.[CrossRef]
    [Google Scholar]
  36. Klösgen, R. B. ( 1997; ). Protein transport into and across the thylakoid membrane. J Photochem Photobiol B: Biology 38, 1-9.[CrossRef]
    [Google Scholar]
  37. Laudenbach, D. E. & Straus, N. A. ( 1988; ). Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170, 5018-5026.
    [Google Scholar]
  38. Michel, K.-P. & Pistorius, E. K. ( 1992; ). Isolation of a photosystem II associated 36 kDa polypeptide and an iron-stress 34 kDa polypeptide from thylakoid membranes of the cyanobacterium Synechococcus PCC 6301 grown under mild iron deficiency. Z Naturforsch 47c, 867-874.
    [Google Scholar]
  39. Michel, K.-P., Thole, H. H. & Pistorius, E. K. ( 1996; ). IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations. Microbiology 142, 2635-2645.[CrossRef]
    [Google Scholar]
  40. Michel, K.-P., Exss-Sonne, P., Scholten-Beck, G., Kahmann, U., Ruppel, H. G. & Pistorius, E. K. ( 1998; ). Immunocytochemical localisation of IdiA, a protein expressed under iron or manganese limitation in the mesophilic cyanobacterium Synechococcus PCC 6301 and the thermophilic cyanobacterium Synechococcus elongatus. Planta 205, 73-81.[CrossRef]
    [Google Scholar]
  41. Michel, K.-P., Krüger, F., Pühler, A. & Pistorius, E. K. ( 1999; ). Molecular characterization of idiA and adjacent genes in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942. Microbiology 145, 1473-1484.[CrossRef]
    [Google Scholar]
  42. Michel, K.-P., Pistorius, E. K. & Golden, S. S. ( 2001; ). Unusual regulatory elements for iron deficiency induction of the idiA gene of Synechococcus elongatus PCC 7942. J Bacteriol 183, 5015-5024.[CrossRef]
    [Google Scholar]
  43. Mietzner, T. A. & Morse, S. A. ( 1994; ). The role of iron-binding proteins in the survival of pathogenic bacteria. Annu Rev Nutr 14, 471-493.[CrossRef]
    [Google Scholar]
  44. Murzin, A. G. ( 1993; ). Can homologous proteins evolve different enzymatic activities? Trends Biochem Sci 18, 403-405.[CrossRef]
    [Google Scholar]
  45. Nielsen, H., Brunak, S. & von Heijne, G. ( 1999; ). Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng 12, 3-9.[CrossRef]
    [Google Scholar]
  46. Nierzwicki-Bauer, S. A., Balkwill, D. L. & Stevens, S. E.Jr ( 1983; ). Three-dimensional ultrastructure of a unicellular cyanobacterium. J Cell Biol 97, 713-722.[CrossRef]
    [Google Scholar]
  47. Omata, T. & Murata, N. ( 1984; ). Isolation and characterization of three types of membranes from the cyanobacterium (blue-green alga) Synechocystis PCC 6714. Arch Microbiol 139, 113-116.
    [Google Scholar]
  48. Park, Y.-I., Sandström, S., Gustafsson, P. & Öquist, G. ( 1999; ). Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation. Mol Microbiol 32, 123-129.[CrossRef]
    [Google Scholar]
  49. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  50. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G. & Pühler, A. ( 1994; ). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73.[CrossRef]
    [Google Scholar]
  51. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goecke, N. M., Olson, B. J. & Klenk, D. C. ( 1985; ). Measurement of protein using bicinchoninic acid. Anal Biochem 150, 76-85.[CrossRef]
    [Google Scholar]
  52. Stephan, D. P., Ruppel, H. G. & Pistorius, E. K. ( 2000; ). Interrelation between cyanophycin synthesis, l-arginine catabolism and photosynthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. Z Naturforsch 55c, 927–942.
    [Google Scholar]
  53. Straus, N. A. ( 1994; ). Iron deprivation: physiology and gene regulation. In The Molecular Biology of Cyanobacteria , pp. 731-750. Edited by D. A. Bryant. Dordrecht: Kluwer.
  54. Tam, R. & Saier, M. H.Jr ( 1993; ). Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57, 320-346.
    [Google Scholar]
  55. Tandeau de Marsac, N. & Houmard, J. ( 1988; ). Complementary chromatic adaptation: physiological conditions and action spectra. Methods Enzymol 167, 318-328.
    [Google Scholar]
  56. von Heijne, G. ( 1986; ). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14, 4683-4690.[CrossRef]
    [Google Scholar]
  57. Webb, E. A., Moffett, J. W. & Waterbury, J. B. ( 2001; ). Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): identification of the IdiA protein. Appl Environ Microbiol 67, 5444-5452.[CrossRef]
    [Google Scholar]
  58. Wenk, S.-O. & Kruip, J. ( 2000; ). Novel, rapid purification of the membrane protein photosystem I by high-performance liquid chromatography on porous materials. J Chromatogr B 737, 131-142.[CrossRef]
    [Google Scholar]
  59. Wexler, M., Bogsch, E. G., Klösgen, R. B., Palmer, T., Robinson, C. & Berks, B. C. ( 1998; ). Targeting signals for a bacterial Sec-independent export system direct plant thylakoid import by the ΔpH pathway. FEBS Lett 431, 339-342.[CrossRef]
    [Google Scholar]
  60. Williams, J. G. K. ( 1988; ). Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis PCC 6803. Methods Enzymol 167, 766-778.
    [Google Scholar]
  61. Zak, E., Norling, B., Maitra, R., Huang, F., Andersson, B. & Pakrasi, H. B. ( 2001; ). The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci USA 98, 13443-13448.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-10-3293
Loading
/content/journal/micro/10.1099/00221287-148-10-3293
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error